Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect
Animals invest crucial resources in foraging to support development, sustenance, and reproduction. Foraging and feeding behaviors are rhythmically expressed by most insects. Rhythmic behaviors are modified by exogenous factors like temperature and photoperiod, and internal factors such as the physio...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2023.1304626/full |
| _version_ | 1797361303484891136 |
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| author | Evan Force Evan Force Michel B. C. Sokolowski Caroline Suray Stéphane Debernard Abhishek Chatterjee Matthieu Dacher Matthieu Dacher |
| author_facet | Evan Force Evan Force Michel B. C. Sokolowski Caroline Suray Stéphane Debernard Abhishek Chatterjee Matthieu Dacher Matthieu Dacher |
| author_sort | Evan Force |
| collection | DOAJ |
| description | Animals invest crucial resources in foraging to support development, sustenance, and reproduction. Foraging and feeding behaviors are rhythmically expressed by most insects. Rhythmic behaviors are modified by exogenous factors like temperature and photoperiod, and internal factors such as the physiological status of the individual. However, the interactions between these factors and the circadian clock to pattern feeding behavior remains elusive. As Drosophila, a standard insect model, spends nearly all its life on food, we rather chose to focus on the adults of a non-model insect, Agrotis ipsilon, a nocturnal cosmopolitan crop pest moth having structured feeding activity. Our study aimed to explore the impact of environmental cues on directly measured feeding behavior rhythms. We took advantage of a new experimental set-up, mimicking an artificial flower, allowing us to specifically monitor feeding behavior in a naturalistic setting, e.g., the need to enter a flower to get food. We show that the frequency of flower visits is under the control of the circadian clock in males and females. Feeding behavior occurs only during the scotophase, informed by internal clock status and external photic input, and females start to visit flowers earlier than males. Shorter duration visits predominate as the night progresses. Importantly, food availability reorganizes the microstructure of feeding behavior, revealing its plasticity. Interestingly, males show a constant number of daily visits during the 5 days of adult life whereas females decrease visitations after the third day of adult life. Taken together, our results provide evidence that the rhythmicity of feeding behavior is sexually dimorphic and controlled by photoperiodic conditions through circadian clock-dependent and independent pathways. In addition, the use of the new experimental set-up provides future opportunities to examine the regulatory mechanisms of feeding behavior paving the way to investigate complex relationships between feeding, mating, and sleep-wake rhythms in insects. |
| first_indexed | 2024-03-08T15:51:56Z |
| format | Article |
| id | doaj.art-b140f132608b41beadba9bd1c80bc7fd |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-03-08T15:51:56Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-b140f132608b41beadba9bd1c80bc7fd2024-01-09T04:35:21ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2024-01-011410.3389/fphys.2023.13046261304626Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insectEvan Force0Evan Force1Michel B. C. Sokolowski2Caroline Suray3Stéphane Debernard4Abhishek Chatterjee5Matthieu Dacher6Matthieu Dacher7Sorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris, Versailles, FranceSorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris, Paris, FranceUniversité de Picardie—Jules Verne, Amiens, FranceSorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris, Versailles, FranceSorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris, Paris, FranceSorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris, Versailles, FranceSorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris, Versailles, FranceSorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris, Paris, FranceAnimals invest crucial resources in foraging to support development, sustenance, and reproduction. Foraging and feeding behaviors are rhythmically expressed by most insects. Rhythmic behaviors are modified by exogenous factors like temperature and photoperiod, and internal factors such as the physiological status of the individual. However, the interactions between these factors and the circadian clock to pattern feeding behavior remains elusive. As Drosophila, a standard insect model, spends nearly all its life on food, we rather chose to focus on the adults of a non-model insect, Agrotis ipsilon, a nocturnal cosmopolitan crop pest moth having structured feeding activity. Our study aimed to explore the impact of environmental cues on directly measured feeding behavior rhythms. We took advantage of a new experimental set-up, mimicking an artificial flower, allowing us to specifically monitor feeding behavior in a naturalistic setting, e.g., the need to enter a flower to get food. We show that the frequency of flower visits is under the control of the circadian clock in males and females. Feeding behavior occurs only during the scotophase, informed by internal clock status and external photic input, and females start to visit flowers earlier than males. Shorter duration visits predominate as the night progresses. Importantly, food availability reorganizes the microstructure of feeding behavior, revealing its plasticity. Interestingly, males show a constant number of daily visits during the 5 days of adult life whereas females decrease visitations after the third day of adult life. Taken together, our results provide evidence that the rhythmicity of feeding behavior is sexually dimorphic and controlled by photoperiodic conditions through circadian clock-dependent and independent pathways. In addition, the use of the new experimental set-up provides future opportunities to examine the regulatory mechanisms of feeding behavior paving the way to investigate complex relationships between feeding, mating, and sleep-wake rhythms in insects.https://www.frontiersin.org/articles/10.3389/fphys.2023.1304626/fullAgrotis ipsilonLepidopterafeeding behaviorcircadian behaviordevelopmental timingautomated feeding cage |
| spellingShingle | Evan Force Evan Force Michel B. C. Sokolowski Caroline Suray Stéphane Debernard Abhishek Chatterjee Matthieu Dacher Matthieu Dacher Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect Frontiers in Physiology Agrotis ipsilon Lepidoptera feeding behavior circadian behavior developmental timing automated feeding cage |
| title | Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect |
| title_full | Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect |
| title_fullStr | Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect |
| title_full_unstemmed | Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect |
| title_short | Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect |
| title_sort | regulation of feeding dynamics by the circadian clock light and sex in an adult nocturnal insect |
| topic | Agrotis ipsilon Lepidoptera feeding behavior circadian behavior developmental timing automated feeding cage |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2023.1304626/full |
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